Cytotoxic effect of plant-derived compounds in in vitro models of BrC.
\r\n\tb. The growth of digital environments which can educate and empower as well as exploit and destroy (mobile learning, STEM education, tablets, etc.).
\r\n\tc. Social, racial, class, and gender-based discriminations that restrict the developmental potential and the prosperity perspectives
\r\n\td. Health hazards and illnesses such as the laters COVID-19 pandemic.
\r\n\te. Armed conflicts with casualties and displacements of populations seeking refuge
\r\n\tf. Lack of physical spaces that will support and nourish development and learning, etc.
\r\n\tEducation in the post-modern era strives to address the above issues and develop policies, curricula, methodologies, and strategies to contribute to an environmentally and socially sustainable future. It embraces multiple perspectives and worldviews and seeks to touch on inequalities and discriminations in favor of equity. In this direction, children’s s agency lies at the heart of democratic approaches. Educational processes adopt forms of interactions that actualize learning as “becoming” and place it in a continuum between past, present, and future. This book intends to feature innovative approaches that employ transformative elements (targets, methods, materials, ideas, etc.) and embrace the concept of child development as “becoming” in an ever-changing and challenging world.
\r\n\r\n\tWe invite authors to contribute original research or research review papers that present innovative approaches addressing personal and social transformation. All aspects of early childhood education will be considered, including research methodology for the early years.
",isbn:"978-1-80355-949-0",printIsbn:"978-1-80355-948-3",pdfIsbn:"978-1-80355-950-6",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!1,isSalesforceBook:!1,isNomenclature:!1,hash:"351c41dca5c8c997f15e758f2e035178",bookSignature:"Dr. Maria Ampartzaki and Associate Prof. Michail Kalogiannakis",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/11281.jpg",keywords:"Early Childhood Education, Preschool, STEAM, Environmental Sustainability, Social Sciences, Social Sustainability, ICT, Digital Devices, Education for Equity, Gender Issues, Post-modern Epistemology, Social Constructivism",numberOfDownloads:65,numberOfWosCitations:0,numberOfCrossrefCitations:0,numberOfDimensionsCitations:0,numberOfTotalCitations:0,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"November 16th 2021",dateEndSecondStepPublish:"December 14th 2021",dateEndThirdStepPublish:"February 12th 2022",dateEndFourthStepPublish:"May 3rd 2022",dateEndFifthStepPublish:"July 2nd 2022",dateConfirmationOfParticipation:null,remainingDaysToSecondStep:"8 months",secondStepPassed:!0,areRegistrationsClosed:!0,currentStepOfPublishingProcess:5,editedByType:null,kuFlag:!1,biosketch:"Dr. Maria Ampartzaki is an Assistant Professor in Early Childhood Education in the Department of Preschool Education at the University of Crete. Her research interests include ICT in education, science education in the early years, inquiry-based and art-based learning, teachers’ professional development, action research, and the Pedagogy of Multiliteracies, among others. She has run and participated in several funded and non-funded projects on the teaching of Science, Social Sciences, and ICT in education.",coeditorOneBiosketch:"Michail Kalogiannakis is an Associate Professor of the Department of Preschool\r\nEducation, University of Crete in Greece. He graduated from the Physics Department\r\nof the University of Crete and continued his post-graduate studies at the University\r\nParis-7 and University Paris-5 and received his Ph.D. degree at the University Paris 5.\r\nHis research interests include science education in early childhood, science teaching\r\nand learning, e-learning, the use of ICT in science education, and games simulations.",coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"422488",title:"Dr.",name:"Maria",middleName:null,surname:"Ampartzaki",slug:"maria-ampartzaki",fullName:"Maria Ampartzaki",profilePictureURL:"https://mts.intechopen.com/storage/users/422488/images/system/422488.jpg",biography:"Dr Maria Ampartzaki is an Assistant Professor in Early Childhood Education in the Department of Preschool Education at the University of Crete. Her research interests include ICT in education, science education in the early years, inquiry-based and art-based learning, teachers’ professional development, action research, and the Pedagogy of Multiliteracies, among others. She has run and participated in several funded and non-funded projects on the teaching of Science, Social Sciences, and ICT in education. She also has the experience of participating in five Erasmus+ projects.",institutionString:"University of Crete",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"0",totalChapterViews:"0",totalEditedBooks:"0",institution:{name:"University of Crete",institutionURL:null,country:{name:"Greece"}}}],coeditorOne:{id:"260066",title:"Associate Prof.",name:"Michail",middleName:null,surname:"Kalogiannakis",slug:"michail-kalogiannakis",fullName:"Michail Kalogiannakis",profilePictureURL:"https://mts.intechopen.com/storage/users/260066/images/system/260066.jpg",biography:"Michail Kalogiannakis is an Associate Professor of the Department of Preschool Education, University of Crete, and an Associate Tutor at School of Humanities at the Hellenic Open University. He graduated from the Physics Department of the University of Crete and continued his post-graduate studies at the University Paris 7-Denis Diderot (D.E.A. in Didactic of Physics), University Paris 5-René Descartes-Sorbonne (D.E.A. in Science Education) and received his Ph.D. degree at the University Paris 5-René Descartes-Sorbonne (PhD in Science Education). His research interests include science education in early childhood, science teaching and learning, e-learning, the use of ICT in science education, games simulations, and mobile learning. 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From chapter submission and review to approval and revision, copyediting and design, until final publication, I work closely with authors and editors to ensure a simple and easy publishing process. I maintain constant and effective communication with authors, editors and reviewers, which allows for a level of personal support that enables contributors to fully commit and concentrate on the chapters they are writing, editing, or reviewing. I assist authors in the preparation of their full chapter submissions and track important deadlines and ensure they are met. I help to coordinate internal processes such as linguistic review, and monitor the technical aspects of the process. As an ASM I am also involved in the acquisition of editors. Whether that be identifying an exceptional author and proposing an editorship collaboration, or contacting researchers who would like the opportunity to work with IntechOpen, I establish and help manage author and editor acquisition and contact."}},relatedBooks:[{type:"book",id:"6942",title:"Global Social Work",subtitle:"Cutting Edge Issues and Critical Reflections",isOpenForSubmission:!1,hash:"222c8a66edfc7a4a6537af7565bcb3de",slug:"global-social-work-cutting-edge-issues-and-critical-reflections",bookSignature:"Bala Raju Nikku",coverURL:"https://cdn.intechopen.com/books/images_new/6942.jpg",editedByType:"Edited by",editors:[{id:"263576",title:"Dr.",name:"Bala",surname:"Nikku",slug:"bala-nikku",fullName:"Bala Nikku"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"6926",title:"Biological Anthropology",subtitle:"Applications and Case Studies",isOpenForSubmission:!1,hash:"5bbb192dffd37a257febf4acfde73bb8",slug:"biological-anthropology-applications-and-case-studies",bookSignature:"Alessio Vovlas",coverURL:"https://cdn.intechopen.com/books/images_new/6926.jpg",editedByType:"Edited by",editors:[{id:"313084",title:"Dr.",name:"Alessio",surname:"Vovlas",slug:"alessio-vovlas",fullName:"Alessio Vovlas"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"1591",title:"Infrared Spectroscopy",subtitle:"Materials Science, Engineering and Technology",isOpenForSubmission:!1,hash:"99b4b7b71a8caeb693ed762b40b017f4",slug:"infrared-spectroscopy-materials-science-engineering-and-technology",bookSignature:"Theophile Theophanides",coverURL:"https://cdn.intechopen.com/books/images_new/1591.jpg",editedByType:"Edited by",editors:[{id:"37194",title:"Dr.",name:"Theophile",surname:"Theophanides",slug:"theophile-theophanides",fullName:"Theophile Theophanides"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"3161",title:"Frontiers in Guided Wave Optics and Optoelectronics",subtitle:null,isOpenForSubmission:!1,hash:"deb44e9c99f82bbce1083abea743146c",slug:"frontiers-in-guided-wave-optics-and-optoelectronics",bookSignature:"Bishnu Pal",coverURL:"https://cdn.intechopen.com/books/images_new/3161.jpg",editedByType:"Edited by",editors:[{id:"4782",title:"Prof.",name:"Bishnu",surname:"Pal",slug:"bishnu-pal",fullName:"Bishnu Pal"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"371",title:"Abiotic Stress in Plants",subtitle:"Mechanisms and Adaptations",isOpenForSubmission:!1,hash:"588466f487e307619849d72389178a74",slug:"abiotic-stress-in-plants-mechanisms-and-adaptations",bookSignature:"Arun Shanker and B. 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Breast cancer [BrC] is the deadliest malignancy in women worldwide and also an important public health problem being the second leading cause of cancer in women accounting for more than 626,679 deaths only in 2018 [2]. In many cases this disease has become fatal because of its multifactorial origin and also because it has a great number of exogenous and endogenous factors that can stimulate different pathways [3]. In early BrC, gene expression profiles are determined for hormone receptor (HR)-positive disease and human epidermal growth factor type 2 receptor (HER2) status which define if a patient is likely to receive systemic therapy and are therefore used to guide their treatment [4]. Approximately 60–70% of primary BrC cases express positive estrogen receptors (ER+) or positive progesterone receptors (PR+) or both and are hormone responsive. However, about 15–20% of BrC cases are in the category of triple-negative phenotype owing to their lack of ER, PR, and amplified HER2. Commonly, ER+ hormone-dependent BrCs have a better prognosis and are often responsive to antihormone therapy [4].
\nBecause of these reasons, the survival rates for BrC have decreased significantly; however, there have been great advancements in new alternative therapies which not only are safer but are also more effective and inexpensive and have minimal side effects [5]. Therapeutic drugs derived from natural compounds have become of great interest since more than 75% of anticancer drugs were designed and developed from plant-derived natural ingredients which have been proven to have anticancer properties with novel mechanisms [6]. In the last 50 years, nearly 200 new chemical compounds have been approved to fight cancer, of which around 50% are molecules of unmodified natural products and their semisynthetic or synthetic derivatives that are safe and profitable [7, 8]. Small organic molecules such as terpenes, flavonoids, alkaloids, lignans, saponins, vitamins, minerals, glycosides, oils, and other secondary metabolites play a significant role in either the inhibition of proliferation, induction of apoptosis, or other mechanisms that may be altered [9, 10]. The structural diversity of natural products and their wide application in therapeutics have always been recognized by pharmaceutical industries [1].
\nThis chapter summarizes the small novel organic molecules obtained from plants and their derivatives, some of which are on the market and others are found in preclinical studies with encouraging results. We also describe some interesting biotechnological associations between some compounds and nanoparticles or other molecules as antibodies that show a novel potential in the treatment of BrC.
\nThe evaluation of the therapeutic potential of novel plant-derived compounds or secondary metabolites, either pure compounds or the mixture of active constituents, can serve as chemotherapeutic agents in BrC. The biological models used for the development of new drugs include in vitro models using BrC cell lines and are divided into estrogen receptor positive (ER+, T47, MCF-7) and ER negative (ER-, MDA-MB-231, MDA-MB-453, SKBR3). MDA-MB-231 or triple-negative breast cancer cell (TNBC) line, estrogen negative (ER-) and progesterone negative (PR-), and HER- are known to be models for metastasis, which are more aggressive, containing a high potential to metastasize, and are unresponsive to antiestrogens [5, 8]. TNBC line is used to investigate the mechanism underlying migration and invasion. It is important to find cancer therapeutic compounds which possess multi-targeted and multifunctional potential with anti-metastasis activity [8, 11]. MCF-7 is the most used cell line with a great number of publications due to the presence of ER+ [9].
\nIn vitro experiments have also been used in different studies, in order to characterize and identify compounds derived from extracts, essential oils, and other extractions. Trypan blue dye, MTT, sulforhodamine B, and lactic dehydrogenase assays constitute some of the most utilized assays used to evaluate the cytotoxic effect of essential oils and/or pure compounds in different cell lines of BrC. In order to characterize morphological changes, biochemical and molecular levels of cell death, proteins that are modified (expression and activation), gene regulation, migration, invasion, and cell division, among other changes, experiments such as staining with hematoxylin and eosin, Western blot, TUNEL, annexin V, qRT-PCR, scratch assay, and cell cycle assays are performed [12].
\nWide varieties of animal model systems are now available to investigate plant-derived compounds in different stages, such as cancer initiation, promotion progression, invasion, and metastasis. These models are also used to comprehend therapeutic response, which represents an essential step between in vitro systems and clinical studies [8, 13]. The in vivo models are also used to investigate the capability of plant formulation to induce an anti-BrC effect where it is sought to optimize dose, bioavailability, administration routes, and selective delivery and reduce toxic effects, among others [8, 14]. The two animal species that will be mentioned in this review are those involving mice and rats [14]; however, BrC mouse models are used in a variety of preclinical studies [13].
\nThere are different types of in vivo models of BrC, such as cell line-derived xenografts (MDA-MB-231 line) that are implanted into immunocompromised animals (cell-derived xenografts, CDX). CDX models represent a relatively homogenous mass of transformed breast epithelial cells, and depending on where the cells are inoculated, they are classified as ectopic CDX (models advanced disease only, subcutaneous injection of human tumor cells), orthotopic CDX (in mammary gland/fat pad), metastatic CDX (following tail vein or intra-cardiac injection in specific sites, i.e., bone or lung), syngeneic (mouse tissue implanted to strain-matched host) or metastasis with syngeneic model (usually fast-growing tumors and microenvironment derive from the same species, i.e., 4T1 cells), and genetically engineered mouse models (GEMMs) to address early events of tumorigenesis [13]. Nonetheless, researchers need to consider the limitations of each model and the mechanism of action of the compound previously investigated in in vitro models.
\nPlants produce bioactive secondary metabolites such as flavonoids [15], terpenoids [1], alkaloids [16], tannins, and others, which have profusely been studied for BrC (1, 8). Here, we describe some terpenoid compounds such as
Molecular targets of plant-derived compounds in BrC.
Source | \nCompound | \nStudy type | \nConcentration | \nRef | \n
---|---|---|---|---|
Apples, herbs and spices including rosemary | \nUrsolic acid (UA) | \nMCF-7, MDA-MB-231 | \n221.39 μg/ml 239.47 μg/ml | \n[33] | \n
Apiaceae family, | \nCynaroside | \nMCF-7 | \nIC50:3.98 μg/ml | \n[42] | \n
Soybeans, soy foods, legumes | \nBiochanin (BA) | \nMCF-7, MDA-MB-231 | \n63.76 μm and 59.76 μm, respectively | \n[44] | \n
Soybeans, soy foods, legumes | \nGinsenoside (Rh2) | \nMCF-7, MDA-MB-231 | \n57.53 μm and 52.53 μm, respectively | \n[44] | \n
Soybeans, soy foods, legumes | \nGinsenoside + biochanin | \nMDA-MB-231 MCF-7 | \n27.68, 25.41 μm; 25.2 μm, and 22.75 μm | \n[44] | \n
Tomatoes ( | \nNaringenin | \nMDA-MB-231 | \n40 μg/ml | \n[43] | \n
Soy products | \nGenistein (GEN) | \nMCF-7, MDA-MB-231 /ERβ1 | \n100 μm | \n[48] | \n
Tomatoes ( | \nLycopene (LYC) | \nMDA-MB-231 MCF-7 | \n≥1.25 μm to 5 μl in TNBC. 50 μm | \n[11, 12] | \n
LYC incorporated biopolymeric nanoparticles with whey protein isolate | \nLycopene (LYC-WPI-NPs) | \nMCF-7 | \n25–50 μm/ml | \n[49] | \n
A derivative from | \nPerillyl alcohol a hydroxylated product of | \nKPL-1, MCF-7, MKL-F, MDA-MB-231 | \n500 μm | \n[26] | \n
\n | \nPaclitaxel | \nMCF-7 T47-D, MBA-MB-231, MDA-MB-435 | \n100–500 nm | \n[28] | \n
\n | \nPaclitaxel-loaded nanospheres | \nMDA-MB-435, ZR.75.1 | \n0.06–0.6 ng/ml | \n[50] | \n
Grapes, wine, nuts, berries | \nResveratrol | \nMCF-7 | \n10–150 μm | \n[51] | \n
\n | \nCamptothecin | \nMDA-MB-231 MCF-7 | \n100 nm IC50:0.65 nm | \n[52, 53] | \n
\n | \nCurcumin | \nMCF-7 MCF-7 MDA-MB-231 | \nIC50: 29 μg/ml IC50: 35 μm IC50: 30 μm | \n[54, 55] | \n
Vinca alkaloids | \nVincristine | \nMCF-7, HeLa | \nIC50: 170 and 50 nmol/L | \n[56] | \n
Cytotoxic effect of plant-derived compounds in in vitro models of BrC.
The anti-BrC activities of plant-derived compounds discussed in this chapter are taken from published articles that demonstrated an anti-BrC activity against specific cancer cell lines (see \nTable 2\n) and in vivo models (see \nTable 3\n) or clinical studies with their mechanism of action.
\nCompound | \nStudy type | \nDose and activity | \nRef | \n
---|---|---|---|
\n | \nDMBA and NMU-induced mammary carcinogenesis in rats | \n10% of limonene diet. Induced complete regression of primary rat mammary tumors and prevented the development of secondary tumors | \n[24] | \n
Perillyl alcohol a hydroxylated product of | \nMammary rat tumor induced with KPL-1 cells | \n75 mg/kg. Suppressed orthotopically transplanted KPL-1 tumor cell growth and regional lymph node metastasis in a nude mouse system | \n[26] | \n
Paclitaxel-encapsulated liposomes | \nDMBA mammary tumor | \n20 mg/kg. In combination with 500 mg/kg of | \n[97] | \n
Paclitaxel-loaded nanospheres | \nTumor xenograft model in mice | \n5–50 mg/kg. Showed an equivalent antitumor efficacy to the clinical formulation and provided a superior safety and improved tolerability to higher paclitaxel doses | \n[50] | \n
Resveratrol | \nDMBA induced mammary cancer in rats estrogen-induced breast carcinoma in rats | \n100 μg/rat. Suppressed COX-2 and matrix metalloprotease-9 expression in the breast tumor. 50 mg. Inhibits breast carcinogenesis via induction of NRF2-mediated protective pathways | \n[67, 98] | \n
Curcumin | \nMCF-7 xenografts mouse breast cancer model | \n100 mg/kg in combination with mitomycin 1–2 mg/kg. The combined treatment inhibited tumor growth, induced G1 arrest, and decreased cyclin D1, cyclin E, cyclin A, CDK2, and CDK4 | \n[99] | \n
Camptothecin | \nMouse 4T1 breast tumor model | \n2 mg/kg in combination with 1.05 mg/kg of doxorubicin. Induced 70% of tumor volume reduction and caspase-3 induction | \n[100] | \n
Compounds evaluated in in vivo model of BrC.
Structures of plant-derived compounds with potential effect in the BrC treatment.
Terpenoids are organic compounds derived from five-carbon units (isoprene) assembled and modified in different ways. The classification of terpenoids is based on the isoprene units which are commonly classified as monoterpenes (C10) and diterpenes (C20), i.e., paclitaxel, and triterpenes as ursolic acid [1]. Interestingly, essential oils are a rich and complex composition of monoterpenes with anti-BrC activity such as
\n
Paclitaxel is a complex diterpene, with a molecular structure of C47H51NO14 and a molecular mass of 853.91 g/mol [18]. This compound induces mitotic arrest and also apoptosis by activating extrinsic or intrinsic pathway. In MCF-7 cells it decreased levels of Bcl-2 protein and increased proapoptotic proteins such as Bax, cytochrome c, caspase-9, and caspase-3 [27, 28]. Likewise, it has also been reported that the induction of apoptosis was independent of caspases [29]. The combination of paclitaxel with a compound that inhibits the mitotic slippage such as phenylethyl isothiocyanate (PEITC) induced apoptosis in MDA-MB-231 cells which are drug resistance [30]. Also, additional activities of taxol have been described including the effect on cell signaling and gene expression and activation of mitogen-activated protein kinases (MAPKs), Raf-1, and protein tyrosine kinases [29]. Paclitaxel has been approved by the FDA to be used alone, or in combination with other anticancer treatments, to treat BrC and other cancers [31, 32].
\nUrsolic acid (3-β-hydroxy-urs-12-en-28-oic acid) is a pentacyclic triterpenoid natural product and a member of the cyclosqualenoid family, commonly named as UA with a molecular structure of C30H48C3 and a molecular mass of 456.7 g/mol [18]. UA is derived from diverse plants and fruits, such as rosemary (
Lycopene (LYC) (trans-lycopene) is a terpene assembled from eight isoprene units and is a rich antioxidant compound, a major carotenoid present in tomatoes (
Essential oils are a complex mixture of secondary metabolites such as monoterpenes that are responsible for their biological activity that includes anti-BrC effect. However, some studies suggested a synergistic activity of the compounds [17]. For example, DBEO was studied on MDA-MB-231 cells.
\nIt had a cytotoxic effect with an IC50 of 53.81 μg/ml. It induced DNA fragmentation and apoptosis via intrinsic pathways due to the activation of Bax, caspase-9, and caspases-3, suggesting a synergistic activity of compounds present in the essential oil, such as 1,5-cyclooctadiene, 3-(methyl-2)propenyl, β-terpineol, 1-(3-methyl-cyclopent-2-enyl)-cyclohexene,
Flavonoids which are polyphenolic substances found in different plant-derived food are divided into flavones (cynaroside), flavonols, flavanones (naringenin), flavanols, isoflavones (genistein (GEN), biochanin A), anthocyanidins, and nonflavonoids [10]. Flavonoids have been reported to have an effect on BrC through numerous mechanisms such as antioxidant, anti-inflammatory, antiproliferative, cytotoxic, anti-angiogenic, and anti-metastatic effects in numerous in vitro and in vivo experiments in estrogen-dependent or estrogen-independent BrC [15, 37] (\nTables 1\n–\n3\n).
\nCynaroside (luteolin-7-
Naringenin (4\',5,7-trihydroxyflavanone) is a flavanone and member of 4\'hydroxyflavanones; it has a molecular structure of C15H12O5 and a molecular mass of 272.256 g/mol [18]. This bioflavonoid is a constituent of tomatoes, citrus fruits, and grapes. Naringenin is a phytoestrogen which is also an important anti-BrC, reported to be involved in decreasing the number of ER-α-positive cells by modulating p38 MAPK signaling pathway [9]. Recently, investigators reported that naringenin has antiproliferative effects by arresting the cell cycle at the G2 phase and caused an inhibitory effect on MDA-MB-231 cells via induction of apoptosis and inhibition of caspase-3 and caspase-9 activities [37, 43].
\nBiochanin or 4\'-methylgenistein (B5,7-dihydroxy-4’-methoxyisoflavone) is an
Also, BA stopped cell growth by blocking the activity of aromatase enzyme which is encoded by the gene CYP19 [5]. On the other hand, ginsenoside Rh2 (protopanaxadiol-type) is the major type of saponin ginsenoside that is separated from
Genistein (4\',5,7-trihydroxyisoflavone) is an isoflavonoid derived from soy products [46]. It has a molecular structure of C15H10O5 and a molecular mass of 270.24 g/mol [18]. This agent has an antineoplastic effect in BrC [47]. GEN inhibits the growth of MDA-MB-231 cells by altering the phosphorylation of proteins included in cell cycle regulation and DNA damage response predominantly, and GEN induced apoptosis via the upregulation of Bax and p21WAF1 proteins in MDA-MB-231 cells and downregulating the expression of caspase-3 [5, 47]. In a recent study, GEN increases cell cycle arrest in G2/M phase in MDA-MB-231/ERβ1 cells, even though there is a high dose of GEN-arrested cells in G0/G1, just like in the MCF-7 cells. Thus, the combinatorial effect of GEN and overexpressed ERβ1 resulted in an active blockade of cell cycle progression and a dramatic inhibition of proliferation in vitro in MCF7 and MDA-MB-231 cells [48]. GEN could be a potential therapeutic agent for ERβ1-positive cancer, which merits further clinical research in the future.
\nResveratrol (3,5,4′-trihydroxy-
Numerous in vitro studies have shown that resveratrol has multiple anticancer effects, which protect the cells against both tumor initiation and cancer progression pathway [9, 57]. The activity of this compound was described in hormone-dependent or non-hormone-dependent BrC cells, in which it was found to induce apoptosis by intrinsic pathway through the upregulation of Bax, Bak, caspase-3, p53, and Akt pathway in different breast cancer cell lines and downregulated Bcl-2 and NF-kB and VEGF [51, 58, 59, 60, 61, 62]. Also, it can induce the extrinsic pathway through the expression of CD95 receptor [63]. A cell surface resveratrol receptor on the extracellular domain of heterodimeric αVβ3-integrin in MCF-7 human BrC cells induces extracellular-regulated kinases 1 and 2 (ERK1/2) and serine-15-p53-dependent phosphorylation leading to a p53-dependent apoptosis [57]. In several in vivo models, resveratrol supplementation was shown to decrease the incidence of mammary tumor formation, tumor volume, metastasis, and induced apoptosis [64, 65, 66]. The effect of resveratrol demonstrated lower tumor growth, decreased angiogenesis, and increased apoptotic index in ERα− and ERβ+ [62]. Also, the following can suppress mammary carcinogenesis in rats induced by DMBA: dietary administration of resveratrol (10 ppm), downregulation of NF-kB, cyclooxygenase-2 and matrix metalloprotease-9 expression in the breast tumor, and decreased tumor incidence [67, 68].
\nThe effect of resveratrol in cancer patients has been investigated in a few clinical trials. The first clinical trial dealing with resveratrol and cancer was performed by Nguyen and collaborators in 2009, through the administration of 0.07 mg/day of resveratrol which resulted in the reduction of Wnt target gene expression, indicating that it may play a beneficial role in the prevention of cancer. These clinical trials have demonstrated resveratrol to be a promising therapeutic and chemopreventive agent [64, 69, 70].
\nCurcumin (1,7-bis(4-hydroxy-3-methoxyphenyl)-1,6-heptadiene-3,5-dione) is an orange-yellow component of turmeric or curry powder; it is a polyphenol natural product isolated from the rhizome of
Alkaloids are a highly diverse group of compounds containing an organic nitrogen atom and a ring structure. Additionally, in most alkaloids the nitrogen atom is located inside the heterocyclic ring structure, which gives them a great biological diversity [16]. The structural diversity of this family is due to the wide number of amino acids used as building blocks [80]. Indeed, the peptide ring that they contain has one or more of its hydrogen atoms replaced with various alkyl radicals, most of which contain oxygen [81, 82]. Consequently, alkaloids can interact with a wide spectrum of molecules. They have a wide distribution in the plant kingdom and are a chemically heterogeneous group of ~17,000 molecules which have displayed pronounced biological and pharmacological activities. Furthermore, several alkaloids exhibit significant biological activities, with their unlimited supply of variable structures as well as their relatively low toxicity and well-documented stability; therefore, alkaloids are being used for their anticancer activity against various cancers [83].
\nCamptothecin is a monoterpene indole alkaloid that consists of five rings [18], commonly named as CPT with a molecular structure of C20H16N2C4 and a molecular mass of 348.35 g/mol [18]. The antitumor activity of this compound is mainly due to its interaction with topoisomerase I (Top1), an enzyme involved in the regulation of DNA topology during replication, recombination, and transcription. It induces cell death by stabilizing a covalent complex between DNA topoisomerase I and the nicked DNA, leading to a DNA lesion [84, 85, 86, 87].
\nCPT antitumoral activity has been reported in different cancer cell lines. Low doses of this compound lead to cell cycle arrest in the G2/M phase and inhibit DNA synthesis but at higher doses cause cell cycle arrest in S phase [52]. Also, the expression of some genes as c-Myc, Bax, BFL1, Bak, pRb2, c-Jun, and Jun-B was upregulated, and Cdk4, cyclin B1, Wee1, CRAF1, and DP1 were downregulated. Among these derivatives, camptothecin-20(s)-
There are some vinca alkaloids in clinical use such as vinblastine, vinorelbine, and vincristine. Many alkaloids have poisonous characteristics but also have physiological effects that make them useful as medications. The oldest group of the plant alkaloids used to treat cancer is the vinca alkaloids. They have a dimeric chemical structure composed of two basic multi-ringed units, an indole nucleus (catharanthine) and a dihydroindole nucleus (vindoline), joined together with other complex systems. Structurally, vincristine and vinblastine are identical except for a single substitution on the vindoline nucleus, where vincristine and vinblastine possess formyl and methyl groups, respectively [90, 91] (\nTable 2\n). The main mechanisms of vinca alkaloid cytotoxicity is due to their interactions with tubulin and disruption of microtubule function, particularly of microtubules comprising the mitotic spindle apparatus, directly causing metaphase arrest. The disturbing effects occur at drug concentrations below those that decrease microtubule mass [91, 92]. Also, disorganization of the microtubule structure provokes the induction of tumor suppressor gene p53 and activation/inactivation of several protein kinases involved in key signaling pathways, including p21, WAF1/CIP1, Ras/Raf, and PKC/PKA, the apoptosis inhibitor Bcl2 and induction of Bax triggering the process of apoptosis in the cell [93]. These alkaloids demonstrated significant antitumor activity in patients with BrC. Also, xenograft mice models were used to evaluate low doses of vinblastine, which resulted in significant but transient xenograft regression, diminishing tumor vascularity, and direct inhibition of angiogenesis. Also, a combination therapy resulted in full and sustained regressions of large established tumors, without an ensuing increase in host toxicity or any signs of acquired drug resistance during treatment [94].
\nThe risk of side effects and multidrug resistance limited the development of vinca alkaloids for clinical applications. To solve these problems, researchers have developed numerous strategies, such as using liposome-entrapped drugs, chemically modified drugs, and polymeric packaging drugs, to reduce the toxicity and enhance the therapeutic efficiency of vinca alkaloids. Many liposome products are still being tested in clinical trials. Another strategy for reducing chemotherapeutic toxicity involves using chemically modified drugs [95, 96].
\nNanotechnology has been found to potentially improve current methods for disease, diagnosis, disease-state imaging, and treatment in BrC.
\nTargeted nanoparticle drug delivery is intended to reduce the side effects of anticancer drugs with both decreasing consumption and treatment expenses, which are the major hurdles in conventional cancer treatment. These small entities can be used in combination with a variety of plant-derived compounds in BrC with a variety of formulations being developed, making them a desirable choice of drug formulation [8].
\nRecently, Jain and collaborators designed and synthesized LYC incorporated with biopolymeric nanoparticles with whey protein isolate nanoparticles (WPI NPs) with encouraging results in the compatibility of LYC-WPI-NPs over plain LYC as an optimum delivery system in vitro because encapsulation process did not affect its anticancer activity even in in vivo tumor model of DMBA where ~57% of LYC group of animals developed tumor compared with ~29% of LYC-WPI-NPs. The new formulation (LYC-WPI-NPs) posed higher cytotoxicity and cellular uptake efficacy as compared to the plain LYC in MCF-7 cells. Antitumoral effect of LYC-WPI-NPs and survival data indicate that proposed formulation strategy is a novel approach for the synchronized delivery of bioactive compound, leading to increased bioavailability, therapeutic efficacy, and safety profiling because of improvement in animal survival (100%), in contrast to animals free of LYC (66.67%) and negative control group (16.67%). This will certainly open new avenues to explore cancer treatment [49].
\nAs a strongly hydrophobic drug, it requires suitable delivery vehicles to effectively distribute into tumor tissues. For efficient distribution of this hydrophobic anticancer drug, paclitaxel is currently formulated and administered to patients via polyethoxylated castor oil (Cremophor EL, CrEL), but it is reported as causing hypersensitivity reactions and neurotoxicity [101]. To date, paclitaxel albumin-bound nanoparticles (Abraxane®) have been approved by the FDA for the treatment of metastatic BrC and non-small cell lung cancer [8]. Nanoparticle-based delivery systems can take advantage of the enhanced permeability and retention (EPR) effect for passive tumor targeting; therefore, they can improve the therapeutic index and decrease the side effects of paclitaxel. In addition, there are a number of novel paclitaxel nanoparticle formulations in clinical trials [50, 101, 102, 103, 104]. Nanoparticle-assisted chemotherapeutic drug delivery has been used because it enhances therapeutic effectiveness. Studies on metastatic BrC demonstrate the inhibition of metastasis by co-delivering chemotherapeutic agent paclitaxel and twist shRNA via complex nanoparticles [105].
\nResearch have concentrated on the development of potential delivery system to increase the aqueous solubility, stability, and bioavailability as well as controlled delivery of camptothecin at or around cancer tissues. For that purpose nanoencapsulation of drugs in a biodegradable polymer has been reported to protect the drug in the core of the polymeric shell [106, 107, 108]. Camptothecin encapsulated in nanoparticles demonstrated antitumor activity in in vitro and in vivo models; in MCF-7 cells the IC50 was lower (0.23 μm) than the pure compound (0.57 μm) [106, 109].
\nAs other compounds, in order to increase photostability and enhance its anticancer activity against BrC cells, scientists have formulated the transferrin-mediated solid lipid nanoparticle, which enhances the anticancer effect of curcumin in BrC cells in vitro [110]. A polymer-drug conjugate called polycurcumins also has advantages of high drug-loading efficiency, fixed drug-loading contents, stabilized curcumin in their backbones, and tailored water solubility. The polycurcumins are cytotoxic to cancer cells, but a polyacetal-based polycurcumin is highly cytotoxic to MCF-7 cells. The effect of these polymers induced cell cycle arrest and apoptosis partially through the caspase-3-dependent pathway. In vivo, this polymer showed antitumor activity in SKOV-3 intraperitoneal xenograft tumor model [111].
\nIn recent years, natural products and their derivatives have been among the major sources of drugs for the treatment of cancer as well as nanoparticles or antibodies. Furthermore, new treatments for different cases of BrC are necessary; this involves linking each cytotoxic drug concerned with a mAb by a linker group to produce a tripartite drug called an “antibody-drug conjugate” (ADC). A means of selective delivery of highly cytotoxic natural products as “prodrugs” to tumor cells has proven necessary in order to reduce off-target effects and increase therapeutic outcomes [8, 112].
\nThe plant-derived compounds are secondary metabolites that have a different mechanism of action; although all of them are cytotoxic for BrC cells, new tools are being sought to increase their effectiveness, with less toxic effects. Also, incorporation of paclitaxel in liposomes can facilitate its delivery to cancer cells and eliminate the adverse reactions associated with the Cremophor EL vehicle. The lipid components of the liposomal formulation were nontoxic, but the intracellular paclitaxel levels were higher when MCF-7 cells were treated with the liposomal paclitaxel formulation; also, liposomal paclitaxel was as effective as conventional paclitaxel in inducing G2/M arrest after 1 day of treatment with 10 mmol/L, increasing the percentage of cells in this population from about 20% in cycling cells to over 60% after 7 days [104].
\nAbraxane® or nanoparticle albumin-bound paclitaxel (nab-paclitaxel) suspension demonstrated greater efficacy with less toxicity than docetaxel in metastatic BrC. This treatment has been approved to reduce toxicity and increased overall survival rates, compared to the parent compound [8]. Nab-paclitaxel is a neoadjuvant chemotherapy in HER2-negative BrC stages I, II, and III.
\nThe recommended dose of Abraxane® is 260 mg/m2 administered intravenously for 30 minutes, every 3 weeks. The results suggest that Abraxane® is effective in patients with highly proliferative cancers (81).
\nIn nature, plants contain secondary metabolites, which have been used by humans to treat different diseases, since they have a complex diversity of chemical structures that have been specifically related to have anti-BrC activity in several preclinical studies with more than one mechanism of action; as a result, they can provide greater degree of efficacy. Several natural compounds are highlighted in this chapter, and their mechanism of action, synergistic action, nano-formulations, and future potentials are widely discussed, and due to the promising potential they represent, in fact, some of them are already used as treatment for BrC. However, it is necessary to have a greater diversity of drugs to be able to treat each one of the different tumors of BrC, since each BrC is different and many of these drugs may still induce several side effects and the development of mechanisms of resistance to drugs must be avoided. Subsequent from this review, we can conclude that although there are many compounds that have been characterized mainly in in vitro models and only around 10–20% of these were also evaluated in in vivo models and less than 10% are being evaluated already in clinical phases, it is essential to conduct more research on these compounds to learn their mechanism of action. Also, in their cellular, biochemical, and molecular levels, clinical effects as well as their genetic toxicities should be investigated sufficiently. Compounds that meet the eligibility criteria in these tests should be taken into clinical trial phase, and they may be administered in combination with other compounds or materials that make their pharmacological effect more efficient, make their arrival to the target site more selective, and guarantee their stability, bioavailability, pharmacokinetics, etc. In conclusion, addressing the study of these compounds in clinical phase is a pressing need.
\nThis work was supported by the Secretaría de Investigación y Posgrado del Instituto Politécnico Nacional Grants SIP20170567 and SIP20196913. CRC is supported by CONACyT and BEIFI, IPN Fellowships.
\nThe authors declare that they have no competing interests.
Nanofibrous scaffolds are one of the most promising materials for skin tissue engineering and wound dressing, because they resemble nanoarchitecture of the native extracellular matrix (for a review, see [1]). Therefore, they can serve as suitable carriers of cells for tissue engineering and also as suitable wound dressings, which are able to protect the wound from external harmful effects, mainly microbial infection, and at the same time, they can keep appropriate moisture and gas exchange at the wound site.
\nNanofibrous scaffolds for skin tissue engineering have been fabricated from a wide range of synthetic and nature-derived polymers, which can be either biostable or degradable within the human body. Biostable synthetic polymers used in nanofiber-based skin regenerative therapies include, for example, polyurethane [2], polydimethylsiloxane [3], polyethylene terephthalate [4], polyethersulfone [5], and also hydrogels such as poly(acrylic acid) (PAA, [6]), poly(methyl methacrylate) (PMMA, [7]), and poly[di(ethylene glycol) methyl ether methacrylate] (PDEGMA, [8]). Degradable synthetic polymers typically include poly(ε-caprolactone) (PCL, [9]) and its copolymers with polylactides (PLCL, [10]), polylactides (PLA, [11]) and their copolymers with polyglycolides (PLGA, [12]), and also so-called auxiliary polymers, such as poly(ethylene glycol) (PEG), poly(ethylene oxide) (PEO, [13]) or poly(vinyl alcohol) (PVA, [14]), which facilitated the electrospinning process and improved the mechanical properties and wettability of the chief polymer. However, the synthetic polymers, although they are well-chemically defined and tailorable, are often bioinert, hydrophobic and thus not promoting cell adhesion, and also not well-adhering to the wound site. Therefore, they need to be combined with other bioactive substances, particularly nature-derived polymers.
\nThis chapter is focused on nature-derived polymers used for fabrication of nanofibrous scaffolds for skin tissue engineering and wound healing. The advantages of most of these polymers are their better bioactivity, flexibility, wettability, and adhesion to the wound site. Similarly as synthetic polymers, also nature-derived polymers can be divided into polymers with none or limited degradability, when implanted into human tissues, and polymers well-degradable in human tissues. The first group includes glucans, such as cellulose, schizophyllan, dextran, starch, and other polysaccharides and proteins, such as pullulan, xylan, alginate, pectin, gum tragacanth, gum arabic, silk fibroin, and sericin. The second group of polymers degradable in human tissues includes collagen and its derivative gelatin, elastin, keratin, glycosaminoglycans such as hyaluronic acid, heparin and chondroitin sulfate, and also polymers not produced in the human body, namely chitosan, gellan gum, zein, and poly(3-hydroxybutyrate-
Some of the polymers degradable in human tissues, such as collagen, gelatin, elastin, keratin, and glycosaminoglycans, contain specific cell-binding motifs in their molecules, for example, specific amino acid sequences in proteins and oligosaccharide domains in glycosaminoglycans, which are recognized by cell adhesion receptors of integrin and non-integrin families (for a review, see [15, 16]). These molecules are often used in allogeneic or xenogeneic form, thus they can be associated with pathogen transmission or immune reaction. However, some synthetic polymers, for example PLA and PCL, have been reported to induce a more pronounced inflammatory reaction than gelatin [17].
\nThis review chapter summarizes earlier and recent knowledge on skin tissue engineering and wound dressing applications, based on nanofibrous scaffolds made of nature-derived polymers, including our results.
\nNature-derived nondegradable polymers or polymers with limited degradability in human tissues include polymers not occurring in the human body and synthesized by other organisms, such as plants, algae, fungi, insects, and bacteria.
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Nanofibrous cellulose can be prepared in three basic forms: bacterial cellulose, which contains cellulose nanofibrils, synthesized by bacteria, nanofibrillar cellulose prepared from plants, particularly from wood, by hydrolysis, oxidation, and mechanical disintegration, and cellulose nanofibers created by electrospinning (for a review, see [19]). For electrospinning, cellulose should be solved. Well-known solvent of cellulose is N-methylmorpholine-N-oxide (NMMO). Another possibility is N-alkylinidazolium-derivate ionic liquid and N,N-dimethylacetamide containing 8 wt% of LiCl. However, any of them did not prove to be a good solvent for needleless electrospinning. The most favorable solvent of cellulose was found to be trifluoroacetic acid (TFA). However, TFA causes severe skin burns and is toxic for aquatic organisms even in low concentrations [20]. These problems, which limit the use of cellulose for creation of electrospun scaffolds for biomedical applications, can be solved by substituting the natural cellulose by its derivatives. The mostly used derivative of cellulose is cellulose acetate (CA), mainly due to its easier solubility and biocompatibility. CA can be dissolved in several solvents, however the best ones for electrospinning proved to be acetic acid (AA), and mixtures of acetone and N,N-dimethylacetamide (DMAC). Some results of successfully spun fibers by needleless electrospinning in our experiments can be found in \nFigure 1\n, demonstrating differences in the fiber morphology. The 95% aqueous mixture of AA showed the best results in comparison with acetone/DMAC mixtures due to production of smoother fibers and lower cytotoxicity.
\nScanning electron microscopy of nanofibrous layers produced by wire needleless electrospinning using different solvents, namely 12 wt% of CA in acetone/DMAC (9:1) (left) or 14 wt% of CA in 95% AA (right).
All the mentioned forms of cellulose have been widely applied as wound dressings releasing various bioactive agents into wounds (antimicrobial, anti-inflammatory, antioxidative agents, cytokines, and growth and angiogenic factors), as transparent wound dressings for direct optical monitoring of wounds, for systemic transdermal drug delivery (analgesics, antiphlogistics, corticoids, and antihypertensives) and for construction of epidermal electronics for monitoring wound healing or physiological status of the organism. Non-degradable nanocellulose has also been used as a temporary carrier for delivery of keratinocytes, dermal fibroblasts, and mesenchymal stem cells into wounds (for a review, see [19]).
\nHowever, for use as direct scaffolds for skin tissue engineering, cellulose should be rendered degradable in human tissues. Cellulose is degradable by cellulase enzymes (exoglucanases and endoglucanases), which hydrolyze 1,4-beta-D-glycosidic linkages. These enzymes are not synthesized in human tissues, but they can be incorporated into cellulose scaffolds in order to degrade them gradually [21, 22]. These enzymes are believed to be non-toxic for mammalian cells [23, 24]. Moreover, the final product of cellulose degradation by these enzymes is glucose, which is a natural nutrient for the cells, by contrast with the acidic by-products of the standard currently used biodegradable PLA or PLGA scaffolds [25]. Another possibility how to use cellulase enzymes in skin tissue engineering (and in tissue engineering in general) is cell sheet technology. First, cells can be grown on the top of non-degradable cellulose substrates. After reaching the cell confluence, self-standing cell sheets can be released by exposure of the cellulose substrates to cellulases. Unlike the proteolytic enzymes conventionally used for detaching cells from their growth supports, cellulases do not disintegrate the extracellular matrix (ECM) formed by cells and do not cleave extracellular parts of cell adhesion receptors binding the ECM [26]. The cell sheets can be then replanted in the wound bed.
\nAnother interesting approach how to render the cellulose degradable was metabolic engineering of
Other approaches how to render the cellulose degradable, at least partially, is its oxidation and other chemical modifications of cellulose, such as its conversion into regenerated cellulose or 2,3-dialdehydecellulose. In addition, cellulose of animal origin, that is, from tunicates, degraded more quickly than plant cellulose. For example, when cellulose films from
\n
Other glucans used for fabrication of nanofibrous scaffolds for skin tissue engineering and wound healing include dextran, starch and pullulan. According to the type of their glycosidic bonds, these polysaccharides belong to α-glucans.
\n\n
Dextran was also used as component of a bilayer scaffold for skin tissue engineering. The upper part of the scaffolds was made of electrospun blend of poly(ε-caprolactone-
Dextran is degradable by dextranases, enzymes hydrolyzing (1 → 6)-alpha-D-glycosidic linkages. This enzyme is produced mainly by bacterial and fungi, but it was also detected in animal and human tissues, namely liver and spleen. Therefore, dextran is often chosen for biomedical applications, particularly drug delivery, because it is slowly degradable in human organism. Dextran molecules with Mw higher than 40 kDa are sequestered in the liver and spleen, and then hydrolyzed by endo- and exodextranases. Dextran molecules with Mw lower than 40 kDa can be eliminated through renal clearance [32]. However, dextran hydrogels implanted subcutaneously or intramuscularly into rats did not show signs of degradation 6 weeks post-implantation and were surrounded by a thin fibrous capsule and some macrophages and giant cells, which is a response typical for a number of non-degradable materials [32].
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The degradability of alginate in human organism is limited. Alginate is naturally degraded by alginate lyases or alginate depolymerases, which have been isolated from marine algae, marine animals, bacteria, fungi, viruses, and other microorganisms, but are not present in the human organism. Degradability of alginate can be increased by its oxidation and at low pH. Also the hydrophilicity and water uptake capacity of alginate can help in its removal from the wound site (for a review, see [48]).
\n\n
Other polysaccharides explored for creation of nanofibrous scaffolds for skin tissue engineering and wound healing are gum tragacanth and gum arabic, both polysaccharides of plant origin, degradable by bacteria and fungi, for example, in soil [57, 58].
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In biomaterial science, silk fibroin is considered to be degradable, but in mammalian organism, this degradation is long-lasting and can take more than 1 year. As a kind of biomaterial approved by the Food and Drug Administration (FDA) for medical use, silk is defined by United States Pharmacopeia as non-degradable for its negligible tensile strength loss
The degradation behavior of fibroin scaffolds depends on the preparation method and structural characteristics, such as processing condition, pore size, and silk fibroin concentration (for a review, see [65]). For example, three-dimensional porous scaffolds prepared from silk fibroin using all-aqueous process degraded within 2–6 months after implantation into muscle pouches of rats, while the scaffolds prepared using an organic solvent, hexafluoroisopropanol (HFIP), persisted beyond 1 year. It was probably due to a lower original silk fibroin concentration, larger pore size, and a higher and more homogeneous cellular infiltration of aqueous-derived scaffolds than in HFIP-derived scaffolds [66].
\nFor skin tissue engineering and wound healing, silk fibroin has been combined with various synthetic and natural polymers and other bioactive substances. The polymers included, for example, PCL, [67], poly(L-lactic acid)-
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Nature-derived polymers degradable in human tissues include, in particular, polymers that are synthesized in the human body and usually act as components of ECM. These polymers are proteins (collagen and its derivative gelatin, elastin, fibrinogen and fibrin, keratin) or polysaccharides in non-sulfated form (hyaluronic acid) and sulfated form (heparin-like glycosaminoglycans). In addition, some natural polymers synthesized by other organisms, such as bacteria, fungi, insects, crustaceans or plants, are degradable in human tissues, because they are susceptible to enzymes present in human tissues, such as lysozyme and esterases. These polymers include chitosan, gellan gum, zein, and PHBV.
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Collagen is one of the most widely used natural proteins for creation of nanofibrous scaffolds for skin tissue engineering and wound healing. However, these scaffolds are usually mechanically weak, and therefore they need crosslinking or blending with synthetic polymers. Collagen crosslinking with conventionally used agents, particularly glutaraldehyde, is associated with the risk of the scaffold cytotoxicity. More benign crosslinkers used recently include, for example, citric acid [95] or quaternary ammonium organosilane, a multifunctional crosslinking agent, which improved the electrospinnability of collagen by reducing its surface tension, endowed the collagen nanofibers with potent antimicrobial activity and promoted the adhesion and metabolic activity of primary human dermal fibroblasts without any cytotoxicity, at least in a lower concentration of 0.1% w/w [97].
\nSynthetic polymers used for combination with collagen in nanofibrous scaffolds included PLA [98], PLGA [99, 100], and particularly PCL, which was either blended with collagen [101, 102, 103, 104] or served as substrate for subsequent deposition of collagen [105]. Collagen has also been combined with natural polymers, such as silk fibroin [73] or chitosan in a form of blends [106] or in a form of bilayered scaffolds, where collagen was electrospun onto the chitosan scaffolds [107]. Collagen was also grafted on the surface of composite electrospun PVA/gelatin/alginate nanofibers [41]. Collagen-based or collagen-containing nanofibers have been loaded with a wide range of bioactive substances, such as vitamin C, vitamin D3, hydrocortisone, insulin, triiodothyronine, and epidermal growth factor [100], transforming growth factor-β1 [102], plant extracts such as
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Similarly as collagen, also gelatin is the most promising for skin tissue engineering and wound healing applications in combination with various synthetic and natural polymers. For example, gelatin was combined with polyurethane [109], PLA [11, 17], and particularly with PCL, where it was incorporated into core-shell PCL/gelatin nanofibers as the core polymer [110] or electrospun independently of PCL using a double-nozzle technique, which resulted in creation of two types of nanofibers in the scaffolds, either mixed [111] or arranged in separate gelatin and PCL layers [112]. Gelatin was also combined with a copolymer of lactic acid and caprolactone P(LLA-CL) in the form of blends [113] or in the form of coaxial nanofibers with P(LLA-CL)/gelatin shell and albumin core containing epidermal growth factor, insulin, hydrocortisone, and retinoic acid [114]. Natural proteins combined with gelatin included dextran [31], pullulan [38], alginate [41], silk fibroin [74], and hyaluronan with chondroitin sulfate [86].
\nFor combination with synthetic and natural polymers, for example, with PCL [115], and chitosan and keratin [116], gelatin was also used in the form of photocrosslinkable gelatin methacrylate hydrogel (GelMA). On PCL nanofibers, GelMA showed a higher decoration level in comparison with native gelatin [116]. Self-standing nanofibrous matrices electrospun from GelMA enabled tuning of their water retention capacity, stiffness, strength, elasticity, and degradation by changing the exposure time to UV light [117].
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Developing a bilayer construct of keratinocytes and fibroblasts on a PLLA nanofibrous membrane with fibrin and collagen hydrogel. Left: schematic design; right: real construct.
Also fibrinogen was used for modification of synthetic polymeric nanofibers in order to enhance the cell adhesion and growth. Nanofibrous scaffolds electrospun from blends of PCL and fibrinogen improved the adhesion, proliferation, and epidermal differentiation of adipose tissue-derived stem cells (ADSCs) in comparison with pure PCL scaffolds. Composite PCL/fibrinogen scaffolds seeded with ADSCs also markedly improved healing of full-thickness excisional wounds created in rats in comparison with acellular dermal matrix or acellular dermal matrix with ADSCs [124].
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In most studies dealing with keratin-containing nanofibers, keratin was combined with other natural or synthetic polymers in order to improve the spinnability of keratin, or to improve the bioactivity of the co-electrospun polymer. For example, in a study by Cruz-Maya
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Hyaluronic acid stimulated infiltration of nanofibrous scaffold composed of hyaluronan, silk fibroin and PCL [75], and can help to promote cell proliferation [129]. Electrospinning of pure hyaluronic acid is not simple because of solubility characteristics of this polymer. Hyaluronic acid is well-soluble in water but less-soluble in most organic solvents, which can be solved by mixtures of solvents as water/ethanol or water/dimethylformamide [130]. Increasing of evaporation and decreasing of solution surface tension by the solvent mixing helps to electrospinning process. Another possibility is electrospinning of hyaluronic acid together with a suitable water-soluble polymer such as PVA [131] or PEO. The solution of pure hyaluronic acid [132] or with relatively small amount of carrier PEO was successfully spun into nanofibrous material by air-assisted electrospinning technology, that is, electroblowing [133]. For creation of nanofibrous scaffolds, hyaluronic acid was also used in combination with PCL [134], PLA [135] or gelatin, chondroitin sulfate and sericin [86].
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However, electrospinning of chitosan is difficult due to its polycationic characters. Due to the presence of amine groups in the chitosan molecule, acidic aqueous solutions are the best solvents for this polymer. The best candidates for solvent system seem to be mixture of acetic acid (AA) and formic acid (FA) or trifluoroacetic acid (TFA); however, TFA is highly toxic. Electrospinning of pure chitosan has very low productivity because it requires very concentrated polymeric solutions [141]. Therefore, for creation of nanofibrous scaffolds for skin tissue engineering, chitosan has been mixed with other natural or synthetic polymers, such as collagen [142], gelatin [143], keratin [116], cellulose [144], pectin [54, 55], silk fibroin [69], PHBV [145], PCL [142], PLA [146], PLGA [147], PEO, [148], and also with PVA, which was used in our studies (\nFigure 3\n). Chitosan has also been mixed with various nanoparticles, such as halloysite nanotubes [149], graphene oxide [150] or nanodiamonds [144]. The reason of all these mixtures was to improve the stability, spinnability, wettability, mechanical properties, and biofunctionality of chitosan-containing scaffolds for skin tissue engineering. Combination of chitosan with various polymers also enabled creation of bilayer scaffolds for reconstruction of two main skin layers, that is, epidermis containing keratinocytes and dermis containing fibroblasts [116, 142]. In order to enhance the antimicrobial and wound healing activity of chitosan, this polymer was electrospun together with extract from Henna leaves [151]. In addition, chitosan nanoparticles have been incorporated in nanofibrous scaffolds as carriers for controlled drug delivery, for example, delivery of growth factors, cytokines and angiogenic factors, such as platelet-derived growth factor [152], granulocyte colony-stimulating factor [153] or angiogenin [147]. Nanofibrous scaffolds promising for skin tissue engineering and wound healing were also prepared directly from chitin, which was electrospun either alone with further modifications with fibronectin, laminin and particularly with type I collagen [154], or in combination with silk fibroin [70].
\nScanning electron microscopy of nanofibrous layers produced by needle electrospinning from PVA/chitosan solution.
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\n
\n
Nanofibrous scaffolds made of nature-derived polymers hold a great promise for skin tissue engineering and wound healing. These scaffolds are created from biological matrices, and from this point of view, they resemble the extracellular matrix more closely than synthetic polymers. Some of these polymers, such as collagen, gelatin, elastin, keratin, nonsulfated and sulfated glycosaminoglycans, and also nonmulberry silk fibroin, contain motifs that are recognized and bound by cell adhesion receptors. Therefore, nature-derived polymers can increase the bioactivity of synthetic polymers, when combined with them in nanofibrous scaffolds. Conversely, synthetic polymers can improve the electrospinnability and mechanical properties of the natural polymers. Similarly as synthetic polymers, nature-derived polymers can be more or less degradable in human tissues. Degradable polymers include collagen, gelatin, elastin, keratin, glycosaminoglycans, but also chitosan, gellan gum and PHBV, that is, polymers produced by other than mammalian organisms. Polymers produced by other organisms, such as bacteria, fungi, algae, plants or insects, are usually nondegradable in human tissues, or their degradability is limited due to lack of appropriate enzymes. These polymers include glucans, such as cellulose or dextran, and other polysaccharides and proteins, such as pullulan, alginate, pectin, and silk fibroin. Well-degradable polymers are recommended as direct scaffolds for tissue engineering, while less-degradable polymers are suitable for “intelligent” wound dressing for drug delivery and cell delivery.
\nThis review article was supported by the Grant Agency of the Czech Republic (grants No. 17-02448S and 17-00885S).
\nAuthors are listed below with their open access chapters linked via author name:
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\\n\\nXin-She Yang 2017, 2018
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